ABB  Vol.4 No.4 A , April 2013
Fc receptors: Cell activators of antibody functions
ABSTRACT

At the onset of an infection early defense systems, such as complement, get into action. Specialized leukocytes (white blood cells) of the innate immune system, including monocytes, macrophages, and neutrophils also participate as a first line of defense against infections. These early responses are rapid but not very specific and are usually not enough to clear completely many infections. The adaptive immune system is also needed to finish the job against many microorganisms. Antibody molecules, produced during the adaptive immune response, are crucial for preventing recurrent infections. Although, IgG antibodies are essential for controlling infections, these molecules do not directly damage the microorganisms they recognize. Today, it is established that leukocytes of the innate immune system are responsible for the protective effects of these antibodies. IgG molecules bind to their cognate antigens and are in turn recognized by specific receptors (Fcγ receptors) on the membrane of leukocytes. Crosslinking these receptors on the surface of leukocytes leads to activation of several effector cell functions. These effector functions are geared toward the destruction of microbial pathogens and the induction of an inflammatory state that is beneficial during infections. However, in autoimmune diseases, antibodies can direct these effector functions against normal tissues and cause severe tissue damage. In recent years, several factors that can modulate the IgG-FcγR interaction have been elucidated. In this review, we describe the main types of Fcγ receptors, and our current view of how antibody variants interact with these receptors to initiate different cell responses. In addition, new findings on the signaling role of individual Fcγ receptors are also discussed.


Cite this paper
Rosales, C. and Uribe-Querol, E. (2013) Fc receptors: Cell activators of antibody functions. Advances in Bioscience and Biotechnology, 4, 21-33. doi: 10.4236/abb.2013.44A004.
References
[1]   Akira, S., Uematsu, S. and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell, 124, 783-801. doi:10.1016/j.cell.2006.02.015

[2]   Kawai, T. and Akira, S. (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity, 34, 637-650. doi:10.1016/j.immuni.2011.05.006

[3]   Iwasaki, A. and Medzhitov, R. (2010) Regulation of adaptive immunity by the innate immune system. Science, 327, 291-295. doi:10.1126/science.1183021

[4]   Ballow, M. (2002) Primary immunodeficiency disorders: Antibody deficiency. Journal of Allergy and Clinical Immunology, 109, 581-591. doi:10.1067/mai.2002.122466

[5]   Rosales, C. (2007) Fc receptor and integrin signaling in phagocytes. Signal Transduction, 7, 386-401. doi:10.1002/sita.200700141

[6]   Tohyama, Y. and Yamamura, H. (2006) Complement-mediated phagocytosis—The role of Syk. IUBMB Life, 58, 304-308. doi:10.1080/15216540600746377

[7]   Heyman, B. (2000) Regulation of antibody responses via antibodies, complement, and Fc receptors. Annual Review of Immunology, 18, 709-737. doi:10.1146/annurev.immunol.18.1.709

[8]   Nimmerjahn, F. and Ravetch, J. (2008) Fcγ receptors as regulators of immune responses. Nature Reviews Immunology, 8, 34-47. doi:10.1038/nri2206

[9]   Powell, M.S. and Hogarth, P.M. (2008) Fc receptors. Advances in Experimental Medicine and Biology, 640, 22- 34. doi:10.1007/978-0-387-09789-3_3

[10]   García-García, E. and Rosales, C. (2009) Fc receptor signaling in leukocytes: Role in host defense and immune regulation. Current Immunology Reviews, 5, 227-242. doi:10.2174/157339509788921229

[11]   Hogarth, P. (2002) Fc receptors are major mediators of antibody based inflammation in autoimmunity. Current Opinion in Immunology, 14, 798-802. doi:10.1016/S0952-7915(02)00409-0

[12]   Takai, T. (2002) Roles of Fc receptors in autoimmunity. Nature Reviews Immunology, 2, 580-592.

[13]   Nimmerjahn, F. and Ravetch, J. (2006) Fcγ receptors: Old friends and new family members. Immunity, 24, 19-28. doi:10.1016/j.immuni.2005.11.010

[14]   Arnold, J., Wormald, M., Sim, R., Rudd, P. and Dwek, R. (2007) The impact of glycosylation on the biological function and structure of human immunoglobulins. Annual Review of Immunology, 25, 21-50. doi:10.1146/annurev.immunol.25.022106.141702

[15]   Jinghua, L., Lorraine, L.M., Kristopher, D.M., Carolyn, M., Terry, W.D.C. and Peter, D.S. (2008) Structural recognition and functional activation of FcγR by innate pentraxins. Nature, 456, 989-992. doi:10.1038/nature07468

[16]   Marnell, L., Mold, C. and Du Clos, T. (2005) C-reactive protein: Ligands, receptors and role in inflammation. Clinical Immunology, 117, 104-111. doi:10.1016/j.clim.2005.08.004

[17]   Anthony, R., Nimmerjahn, F., Ashline, D., Reinhold, V., Paulson, J. and Ravetch, J. (2008) Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science, 320, 373-376. doi:10.1126/science.1154315

[18]   Kaneko, Y., Nimmerjahn, F. and Ravetch, J. (2006) Anti- inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science, 313, 670-673. doi:10.1126/science.1129594

[19]   Nimmerjahn, F. and Ravetch, J. (2008) Anti-inflammatory actions of intravenous immunoglobulin. Annual Review of Immunology, 26, 513-533. doi:10.1146/annurev.immunol.26.021607.090232

[20]   Jones, S.L., Lindberg, F.P. and Brown, E.J. (1999) Phagocytosis. In: Paul, W.E., Ed., Fundamental Immunology, Lippincott-Raven Publishers, Philadelphia, 997-1020.

[21]   Sánchez-Mejorada, G. and Rosales, C. (1998) Signal transduction by immunoglobulin Fc receptors. Journal of Leukocyte Biology, 63, 521-533.

[22]   Ravetch, J.V. and Bolland, S. (2001) IgG Fc receptors. Annual Review of Immunology, 19, 275-290. doi:10.1146/annurev.immunol.19.1.275

[23]   Ravetch, J.V. (2003) Fc receptors. In: Paul, W.E., Ed., Fundamental Immunology, Lippincott Williams & Wilkins, Philadelphia, 631-684.

[24]   Fodor, S., Jakus, Z. and Mócsai, A. (2006) ITAM-based signaling beyond the adaptive immune response. Immunology Letters, 104, 29-37. doi:10.1016/j.imlet.2005.11.001

[25]   Underhill, D.M. and Goodridge, H.S. (2007) The many faces of ITAMs. Trends in Immunology, 28, 66-73. doi:10.1016/j.it.2006.12.004

[26]   Tridandapani, S., Siefker, K., Teillaud, J.-L., Carter, J.E., Wewers, M.D. and Anderson, C.L. (2002) Regulated expression and inhibitory function of FcγRIIb in human monocytic cells. The Journal of Biological Chemistry, 277, 5082-5089. doi:10.1074/jbc.M110277200

[27]   Daëron, M. and Lesourne, R. (2006) Negative signaling in Fc receptor complexes. Advances in Immunology, 89, 39-86. doi:10.1016/S0065-2776(05)89002-9

[28]   Willcocks, L.C., Smith, K.G. and Clatworthy, M.R. (2009) Low-affinity Fcγ receptors, autoimmunity and infection. Expert Reviews in Molecular Medicine, 11, e24. doi:10.1017/S1462399409001161

[29]   Nimmerjahn, F., Bruhns, P., Horiuchi, K. and Ravetch, J. (2005) FcγRIV: A novel FcR with distinct IgG subclass specificity. Immunity, 23, 41-51. doi:10.1016/j.immuni.2005.05.010

[30]   Stefanescu, R.N., Olferiev, M., Liu, Y. and Pricop, L. (2004) Inhibitory Fc gamma receptors: From gene to disease. Journal of Clinical Immunology, 24, 315-326. doi:10.1023/B:JOCI.0000029105.47772.04

[31]   Boruchov, A., Heller, G., Veri, M., Bonvini, E., Ravetch, J. and Young, J. (2005) Activating and inhibitory IgG Fc receptors on human DCs mediate opposing functions. The Journal of Clinical Investigation, 115, 2914-2923. doi:10.1172/JCI24772

[32]   Anderson, C. and Grey, H. (1974) Receptors for aggregated IgG on mouse lymphocytes: Their presence on thymocytes, thymus-derived, and bone marrow-derived lymphocytes. The Journal of Experimental Medicine, 139, 1175-1188. doi:10.1084/jem.139.5.1175

[33]   Leclerc, J., Plater, C. and Fridman, W. (1977) The role of the Fc receptor (FcR) of thymus-derived lymphocytes. I. Presence of FcR on cytotoxic lymphocytes and absence of direct role in cytotoxicity. European Journal of Immunology, 7, 543-548.doi:10.1002/eji.1830070810

[34]   Stout, R.D. and Herzenberg, L.A. (1975) The Fc receptor on thymus-derived lymphocytes. I. detection of a subpopulation of murine T lymphocytes bearing the Fc receptor. The Journal of Experimental Medicine, 142, 611- 621. doi:10.1084/jem.142.3.611

[35]   Rajendran, L. and Simons, K. (2005) Lipid rafts and membrane dynamics. Journal of Cell Science, 118, 1099-1102. doi:10.1242/jcs.01681

[36]   Bezman, N. and Koretzky, G.A. (2007) Compartamentalization of ITAM and integrin signaling by adapter molecules. Immunology Review, 218, 9-28. doi:10.1111/j.1600-065X.2007.00541.x

[37]   Newbrough, S.A., Mocsai, A., Clemens, R.A., Wu, J.N., Silverman, M.A., Singer, A.L., Lowell, C.A. and Koretzky, G.A. (2003) SLP-76 regulates Fcγ receptor and integrin signaling in neutrophils. Immunity, 19, 761-769. doi:10.1016/S1074-7613(03)00305-4

[38]   Myung, P.S., Clements, J.L., White, D.W., Malik, Z.A., Cowdery, J.S., Allen, L.-A.H., Harty, J.T., Kusner, D.J. and Koretzky, G.A. (2000) In vitro and in vivo macrophage function can occur independently of SLP-76. International Immunology, 12, 887-897. doi:10.1093/intimm/12.6.887

[39]   Nichols, K.E., Haines, K., Myung, P.S., Newbrough, S., Myers, E., Jumaa, H., Shedlock, D.J., Shen, H. and Koretzky, G.A. (2004) Macrophage activation and Fcγ receptor-mediated signaling do not require expression of the SLP-76 and SLP-65 adaptors. Journal of Leukocyte Biology, 75, 541-552. doi:10.1189/jlb.0703312

[40]   Tridandapani, S., Lyden, T.W., Smith, J.L., Carter, J.E., Coggeshall, K.M. and Anderson, C.L. (2000) The adapter protein LAT enhances Fcγ Receptor-mediated signal transduction in myeloid cells. The Journal of Biological Chemistry, 275, 20480-20487. doi:10.1074/jbc.M909462199

[41]   Daëron, M., Latour, S., Malbec, O., Espinosa, E., Pina, P., Pasmans, S. and Fridman, W.H. (1995) The same tyrosine-based inhibition motif, in the intracytoplasmic domain of FcγRIIB, regulates negatively BCR-, TCR-, and FcR-dependent cell activation. Immunity, 3, 635-646. doi:10.1016/1074-7613(95)90134-5

[42]   Bolland, S. and Ravetch, J. (2000) Spontaneous autoimmune disease in FcγRIIB-deficient mice results from strain-specific epistasis. Immunity, 13, 277-285. doi:10.1016/S1074-7613(00)00027-3

[43]   Takai, T., Ono, M., Hikida, M., Ohmori, H. and Ravetch, J. (1996) Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature, 379, 346-349. doi:10.1038/379346a0

[44]   Dhodapkar, K., Banerjee, D., Connolly, J., Kukreja, A., Matayeva, E., Veri, M., Ravetch, J., Steinman, R. and Dhodapkar, M. (2007) Selective blockade of the inhibitory Fcγ receptor (FcγRIIB) in human dendritic cells and monocytes induces a type I interferon response program. The Journal of Experimental Medicine, 204, 1359-1369. doi:10.1084/jem.20062545

[45]   Dhodapkar, K., Kaufman, J., Ehlers, M., Banerjee, D., Bonvini, E., Koenig, S., Steinman, R., Ravetch, J. and Dhodapkar, M. (2005) Selective blockade of inhibitory Fcgamma receptor enables human dendritic cell maturation with IL-12p70 production and immunity to antibody-coated tumor cells. Proceedings of the National Academy of Sciences of the United States of America, 102, 2910-2915. doi:10.1073/pnas.0500014102

[46]   Kalergis, A. and Ravetch, J. (2002) Inducing tumor immunity through the selective engagement of activating Fc gamma receptors on dendritic cells. The Journal of Experimental Medicine, 195, 1653-1659. doi:10.1084/jem.20020338

[47]   Nimmerjahn, F. and Ravetch, J.V. (2010) Antibody-mediated modulation of immune responses. Immunology Review, 236, 265-275. doi:10.1111/j.1600-065X.2010.00910.x

[48]   Hirano, M., Davis, R.S., Fine, W.D., Nakamura, S., Shimizu, K.Y., H., kato, K., Stephan, R.P. and Cooper, M.D. (2007) IgEb immune complexes activate macrophages through FcγRIV binding. Nature Immunology, 8, 762-771. doi:10.1038/ni1477

[49]   Mancardi, D., Iannascoli, B., Hoos, S., England, P., Daëron, M. and Bruhns, P. (2008) FcγRIV is a mouse IgE receptor that resembles macrophage FcεRI in humans and promotes IgE-induced lung inflammation. The Journal of Clinical Investigation, 118, 3738-3750. doi:10.1172/JCI36452

[50]   Salmon, J.E., Edberg, J.C., Brogle, N.L. and Kimberly, R.P. (1992) Allelic polimorphisms of human Fcγ receptor IIA and Fcγ receptor IIIB. Independent mechanisms for differences in human phagocyte function. The Journal of Clinical Investigation, 89, 1274-1281. doi:10.1172/JCI115712

[51]   Tax, W.J.M., Willems, H.W., Reekers, P.P.M., Capel, P.J.A. and Koene, R.A.P. (1983) Polymorphism in mitogenic effect of IgG1 monoclonal antibodies against T3 antigen on human T cells. Nature, 304, 445-447. doi:10.1038/304445a0

[52]   Koene, H.R., Kleijer, M., Swaak, A.J.G., Sullivan, K.E., Bijl, M., Petri, M.A., Kallenberg, C.G.M., Roos, D., von dem Borne, A.E.G.K. and de Haas, M. (1998) The FcγRIIIA-158F allele is a risk factor for systemic lupus erythematosus. Arthritis & Rheumatism, 41, 1813-1818. doi:10.1002/1529-0131(199810)41:10<1813::AID-ART13>3.0.CO;2-6

[53]   Wu, J., Edberg, J.C., Redecha, P.B., Bansal, V., Guyre, P.M., Coleman, K., Salmon, J.E. and Kimberly, R.P. (1997) A novel polymorphism of FcγRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. The Journal of Clinical Investigation, 100, 1059-1070. doi:10.1172/JCI119616

[54]   Huizinga, T.W.J., Kleijer, M., Tetteroo, P.A.T., Roos, D. and von dem Borne, A.E.G.K. (1990) Biallelic neutrophil Na-antigen system is associated with a polymorphism on the phospho-inositol-linked Fcγ receptor III (CD16). Blood, 75, 213-217.

[55]   Hatta, Y., Tsuchiya, N., Ohashi, J., Matsushita, M., Fujiwara, K., Hagiwara, K., Juji, T. and Tokunaga, K. (1999) Association of Fc gamma receptor IIIB, but not of Fc gamma receptor IIA and IIIA, polymorphisms with systemic lupus erythematosus in Japanese. Genes & Immunity, 1, 53-60. doi:10.1038/sj.gene.6363639

[56]   Salmon, J.E., Edberg, J.C. and Kimberly, R.P. (1990) Fcγ receptor III on human neutrophils. Allelic variants have functionally distinct capacities. The Journal of Clinical Investigation, 85, 1287-1295. doi:10.1172/JCI114566

[57]   Bruhns, P., Iannascoli, B., England, P., Mancardi, D., Fernandez, N., Jorieux, S. and Daëron, M. (2009) Specificity and affinity of human Fcγ receptors and their polymorphic variants for human IgG subclasses. Blood, 113, 3716-3725. doi:10.1182/blood-2008-09-179754

[58]   Uchida, J., Hamaguchi, Y., Oliver, J., Ravetch, J., Poe, J., Haas, K. and Tedder, T. (2004) The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. The Journal of Experimental Medicine, 199, 1659-1669. doi:10.1084/jem.20040119

[59]   Lambert, S., Okada, C. and Levy, R. (2004) TCR vaccines against a murine T cell lymphoma: a primary role for antibodies of the IgG2c class in tumor protection. The Journal of Immunology, 172, 929-936.

[60]   Fossati-Jimack, L., Ioan-Facsinay, A., Reininger, L., Chicheportiche, Y., Watanabe, N., Saito, T., Hofhuis, F.M., Gessner, J.E., Schiller, C., Schmidt, R.E., Honjo, T., Verbeek, J.S. and Izui, S. (2000) Markedly different pathogenicity of four immunoglobulin G isotype-switch variants of an anti-erythrocyte autoantibody is based on their capacity to interact in vivo with the low-affinity Fcγ receptor III. The Journal of Experimental Medicine, 191, 1293-1302. doi:10.1084/jem.191.8.1293

[61]   Nimmerjahn, F. and Ravetch, J. (2005) Divergent immunoglobulin G subclass activity through selective Fc receptor binding. Science, 310, 1510-1512. doi:10.1126/science.1118948

[62]   Markine-Goriaynoff, D. and Coutelier, J. (2002) Increased efficacy of the immunoglobulin G2a subclass in antibody-mediated protection against lactate dehydrogenase-elevating virus-induced polioencephalomyelitis revealed with switch mutants. Journal of Virology, 76, 432- 435. doi:10.1128/JVI.76.1.432-435.2002

[63]   Giorgini, A., Brown, H.J., Lock, H.R., Nimmerjahn, F., Ravetch, J.V., Verbeek, J.S., Sacks, S.H. and Robson, M.G. (2008) FcγRIII and FcγRIV are indispensable for acute glomerular inflammation induced by switch variant monoclonal antibodies. The Journal of Immunology, 181, 8745-8752.

[64]   Daëron, M. (1997) Fc receptor biology. Annual Review of Immunology, 15, 203-234. doi:10.1146/annurev.immunol.15.1.203

[65]   Ravetch, J.V. and Kinet, J.P. (1991) Fc receptors. Annual Review of Immunology, 9, 457-492. doi:10.1146/annurev.iy.09.040191.002325

[66]   Meyer, D., Schiller, C., Westermann, J., Izui, S., Hazenbos, W., Verbeek, J., Schmidt, R. and Gessner, J. (1998) FcγRIII (CD16)-deficient mice show IgG isotype-dependent protection to experimental autoimmune hemolytic anemia. Blood, 92, 3997-4002.

[67]   Baudino, L., Nimmerjahn, F., Azeredo da Silveira, S., Martinez-Soria, E., Saito, T., Carroll, M., Ravetch, J., Verbeek, J. and Izui, S. (2008) Differential contribution of three activating IgG Fc receptors (FcγRI, FcγRIII, and FcγRIV) to IgG2a- and IgG2b-induced autoimmune hemolytic anemia in mice. The Journal of Immunology, 118, 1948-1953.

[68]   Ioan-Facsinay, A., de Kimpe, S., Hellwig, S., van Lent, P., Hofhuis, F., van Ojik, H., Sedlik, C., da Silveira, S., Gerber, J., de Jong, Y., Roozendaal, R., Aarden, L., van den Berg, W., Saito, T., Mosser, D., Amigorena, S., Izui, S., van Ommen, G., van Vugt, M., van de Winkel, J. and Verbeek, J. (2002) Fcγ RI (CD64) contributes substantially to severity of arthritis, hypersensitivity responses, and protection from bacterial infection. Immunity, 16, 391- 402. doi:10.1016/S1074-7613(02)00294-7

[69]   Hamaguchi, Y., Xiu, Y., Komura, K., Nimmerjahn, F. and Tedder, T.F. (2006) Antibody isotype-specific engagement of Fcγ receptors regulate B lymphocyte depletion during CD20 immunotherapy. The Journal of Experimental Medicine, 203, 743-753. doi:10.1084/jem.20052283

[70]   Kaneko, Y., Nimmerjahn, F., Madaio, M. and Ravetch, J. (2006) Pathology and protection in nephrotoxic nephritis is determined by selective engagement of specific Fc receptors. The Journal of Experimental Medicine, 203, 789- 797. doi:10.1084/jem.20051900

[71]   Syed, S., Konrad, S., Wiege, K., Nieswandt, B., Nimmerjahn, F., Schmidt, R. and Gessner, J. (2009) Both FcγRIV and FcγRIII are essential receptors mediating type II and type III autoimmune responses via FcRγ-LAT- dependent generation of C5a. European Journal of Immunology, 39, 3343-3356. doi:10.1002/eji.200939884

[72]   Pricop, L., Redecha, P., Teillaud, J.-L., Frey, J., Fridman, W.H., Sautès-Fridman, C. and Salmon, J.E. (2001) Differential modulation of stimulatory and inhibitory Fcγ receptors on human monocytes by Th1 and Th2 cytokines. The Journal of Immunology, 166, 531-537.

[73]   Schmidt, R. and Gessner, J. (2005) Fc receptors and their interaction with complement in autoimmunity. Immunology Letters, 100, 56-67. doi:10.1016/j.imlet.2005.06.022

[74]   Tridandapani, S., Wardrop, R., Baran, C.P., Wang, Y., Opalek, J.M., Caligiuri, M.A. and Marsh, C.B. (2003) TGF-β1 suppresses myeloid Fcγ receptor function by regulating the expression and function of the common γ-subunit. The Journal of Immunology, 170, 4572-4577.

[75]   Salmon, J.E., Browle, N.L., Edberg, J.C. and Kimberly, R.P. (1991) Fcγ receptor III induces actin polymerization in human neutrophils and primes phagocytosis mediated by Fcγ receptor II. The Journal of Immunology, 146, 997-1004.

[76]   Kocher, M., Siegel, M.E., Edberg, J.C. and Kimberly, R.P. (1997) Cross-linking of Fcγ receptor IIa and Fcγ receptor IIIb induces different proadhesive phenotypes on human neutrophils. The Journal of Immunology, 159, 3940-3948.

[77]   Ortiz-Stern, A. and Rosales, C. (2005) FcγRIIIB stimulation promotes β1 integrin activation in human neutrophils. Journal of Leukocyte Biology, 77, 787-799. doi:10.1189/jlb.0504310

[78]   Rivas-Fuentes, S., García-García, E., Nieto-Castañeda, G. and Rosales, C. (2010) Fcγ receptors exhibit different phagocytosis potential in human neutrophils. Cellular Immunology, 263, 114-121. doi:10.1016/j.cellimm.2010.03.006

[79]   García-García, E., Nieto-Castañeda, G., Ruiz-Saldaña, M., Mora, N. and Rosales, C. (2009) FcγRIIA and FcγRIIIB mediate nuclear factor activation through separate signaling pathways in human neutrophils. The Journal of Immunology, 182, 4547-4556. doi:10.4049/jimmunol.0801468

[80]   Shields, R., Namenuk, A., Hong, K., Meng, Y., Rae, J., Briggs, J., Xie, D., Lai, J., Stadlen, A., Li, B., Fox, J. and Presta, L. (2001) High resolution mapping of the binding site on human IgG1 for FcγRI, FcγRII, FcγRIII, and FcRn and design of IgG1 variants with improved binding to the FcγR. The Journal of Biological Chemistry, 276, 6591- 6604. doi:10.1074/jbc.M009483200

[81]   Mizuochi, T., Hamako, J., Nose, M. and Titani, K. (1990) Structural changes in the oligosaccharide chains of IgG in autoimmune MRL/Mp-lpr/lpr mice. The Journal of Immunology, 145, 1794-1798.

[82]   Rook, G., Steele, J., Brealey, R., Whyte, A., Isenberg, D., Sumar, N., Nelson, J., Bodman, K., Young, A. and Roitt, I. (1991) Changes in IgG glycoform levels are associated with remission of arthritis during pregnancy. Journal of Autoimmunity, 4, 779-794. doi:10.1016/0896-8411(91)90173-A

[83]   van de Geijn, F., Wuhrer, M., Selman, M., Willemsen, S., de Man, Y., Deelder, A., Hazes, J. and Dolhain, R. (2009) Immunoglobulin G galactosylation and sialylation are associated with pregnancy-induced improvement of rheumatoid arthritis and the postpartum flare: results from a large prospective cohort study. Arthritis Research & Therapy, 11, R193. doi:10.1186/ar2892

[84]   Jefferis, R. (2009) Glycosylation as a strategy to improve antibody-based therapeutics. Nature Reviews Drug Discovery, 8, 226-234. doi:10.1038/nrd2804

[85]   Shinkawa, T., Nakamura, K., Yamane, N., Shoji-Hosaka, E., Kanda, Y., Sakurada, M., Uchida, K., Anazawa, H., Satoh, M., Yamasaki, M., Hanai, N. and Shitara, K. (2003) The absence of fucose but not the presence of galactose or bisecting N-acetylglucosamine of human IgG1 complex-type oligosaccharides shows the critical role of enhancing antibody-dependent cellular cytotoxicity. The Journal of Biological Chemistry, 278, 3466-3473. doi:10.1074/jbc.M210665200

[86]   Shields, R., Lai, J., Keck, R., O’Connell, L., Hong, K., Meng, Y., Weikert, S. and Presta, L. (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human FcγRIII and antibody-dependent cellular toxicity. The Journal of Biological Chemistry, 277, 26733-26740. doi:10.1074/jbc.M202069200

[87]   Anthony, R., Wermeling, F., Karlsson, M. and Ravetch, J. (2008) Identification of a receptor required for the anti-inflammatory activity of IVIG. Proceedings of the National Academy of Sciences of the United States of America, 105, 19571-19578. doi:10.1073/pnas.0810163105

[88]   Scallon, B., Tam, S., McCarthy, S., Cai, A. and Raju, T. (2007) Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Molecular Immunology, 44, 1524-1532. doi:10.1016/j.molimm.2006.09.005

[89]   Bruhns, P., Samuelsson, A., Pollard, J. and Ravetch, J. (2003) Colony-stimulating factor-1-dependent macrophages are responsible for IVIG protection in antibody-induced autoimmune disease. Immunity, 18, 573-581. doi:10.1016/S1074-7613(03)00080-3

[90]   Tackenberg, B., Jelcic, I., Baerenwaldt, A., Oertel, W.H., Sommer, N., Nimmerjahn, F. and Lunemann, J.D. (2009) Impaired inhibitory FcγRIIB expression on B cells in chronic inflammatory demyelinating polyneuropathy. Proceedings of the National Academy of Sciences of the United States of America, 106, 4788-4792. doi:10.1073/pnas.0807319106

[91]   Agrawal, A., Singh, P., Bottazzi, B., Garlanda, C. and Mantovani, A. (2009) Pattern recognition by pentraxins. Advances in Experimental Medicine and Biology, 653, 98- 116. doi:10.1007/978-1-4419-0901-5_7

[92]   Bharadwaj, D., Mold, C., Markham, E. and Du Clos, T. (2001) Serum amyloid P component binds to Fc gamma receptors and opsonizes particles for phagocytosis. The Journal of Immunology, 166, 6735-6741.

[93]   Lu, J., Marnell, L., Marjon, K., Mold, C., Du Clos, T. and Sun, P. (2008) Structural recognition and functional activation of FcγR by innate pentraxins. Nature, 456, 989- 992. doi:10.1038/nature07468

[94]   Marjon, K., Marnell, L., Mold, C. and Du Clos, T. (2009) Macrophages activated by C-reactive protein through Fcγ RI transfer suppression of immune thrombocytopenia. The Journal of Immunology, 182, 1397-1403.

[95]   Thomas-Rudolph, D., Du Clos, T., Snapper, C. and Mold, C. (2007) C-reactive protein enhances immunity to Streptococcus pneumoniae by targeting uptake to FcγR on dendritic cells. The Journal of Immunology, 178, 7283-7291.

[96]   Bharadwaj, D., Stein, M., Volzer, M., Mold, C. and Du Clos, T. (1999) The major receptor for C-reactive protein on leukocytes is Fc gamma receptor II. The Journal of Experimental Medicine, 190, 585-590. doi:10.1084/jem.190.4.585

[97]   Rodriguez, W., Mold, C., Kataranovski, M., Hutt, J., Marnell, L., Verbeek, J. and Du Clos, T. (2007) C-reactive protein-mediated suppression of nephrotoxic nephritis: Role of macrophages, complement, and Fcγ receptors. The Journal of Immunology, 178, 530-538.

 
 
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